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Open Access 01-12-2024 | Zika Virus | Research

Associations between the social environment and early childhood developmental outcomes of Puerto Rican children with prenatal Zika virus exposure: a cross-sectional study

Authors: Mary Rodríguez-Rabassa, Allison A. Appleton, Viviana Rosario-Villafañe, Irelis Repollet-Carrer, Marilyn Borges-Rodríguez, Lydiet Dedós-Peña, Marielly González, Paola Velázquez-González, Kamalich Muniz-Rodriguez, Claudia Mántaras-Ortiz, Vanessa Rivera-Amill, Odette Olivieri-Ramos, Luisa I. Alvarado-Domenech

Published in: BMC Pediatrics | Issue 1/2024

Abstract

Background

Prenatal exposure to the Zika virus can lead to microcephaly and adverse developmental outcomes, even in children without evident birth defects. The social environment plays a crucial role in infant health and developmental trajectories, especially during periods of heightened brain plasticity. The study aimed to assess socioenvironmental factors as predictors of developmental outcomes of 36-month-old children exposed to Zika virus prenatally.

Study design

This cross-sectional study included 53 mothers and 55 children enrolled in the Pediatric Outcomes of Prenatal Zika Exposure cohort study in Puerto Rico. The study performs follow-up developmental assessments of children born to mothers with confirmed and probable Zika virus infection during pregnancy. Mothers completed socioenvironmental questionnaires (e.g., Perceived Neighborhood Scale and US Household Food Insecurity Survey). Children’s developmental outcomes were assessed with the Bayley Scales of Infant and Toddler Development: Third Edition, the Ages and Stages Questionnaires: Third Edition, the Ages and Stages Questionnaire-Socioemotional: Second Edition, and the Child Adjustment and Parent Efficacy Scale.

Results

Linear regression models, adjusting for a child’s sex and age and maternal education, revealed that early life exposure to food insecurity and maternal pregnancy stressors were significantly associated with poorer developmental outcomes in Zika virus-exposed children at 36 months of age. Maternal resilience representation of adaptive ability was associated with the preservation of adequate developmental outcomes in children.

Conclusions

Pregnancy and early childhood are critical life periods for ensuring optimal brain development in children. While the mechanisms in the interaction of children with their environment are complex, the risk and protective factors identified in the study are modifiable through public policy and preventive initiatives. Implementation of comprehensive strategies that improve access to social support programs, educational and nutritional interventions, and mental health services during pregnancy and early childhood can enhance the developmental potential of vulnerable children.

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Bick J, Nelson CA. Early adverse experiences and the developing brain. Neuropsychopharmacol. 2016;41(1):177–96.CrossRef

Garner A, Yogman M, Committee on Psychosocial Aspects of Child and Family Health, Section on Developmental, and Behavioral Pediatrics, Council on Early Childhood. Preventing childhood toxic stress: partnering with families and communities to promote relational health. Pediatrics. 2021;148(2):e2021052582.PubMedCrossRef

National Scientific Council on the Developing Child. Place matters: The environment we create shapes the foundations of healthy development: Working paper No. 16. 2023. https://developingchild.harvard.edu/place-matters-the-environment-we-create-shapes-the-foundations-of-healthy-development/. Accessed 8 August 2023.

Shonkoff JP, Boyce WT, McEwen BS. Neuroscience, molecular biology, and the childhood roots of health disparities: building a new framework for health promotion and disease prevention. JAMA. 2009;301(21):2252–9.PubMedCrossRef

Fortin O, Mulkey SB. Neurodevelopmental outcomes in congenital and perinatal infections. Curr Opin Infect Dis. 2023;36(5):405–13.PubMedCrossRef

Alvarado-Domenech LI, Rivera-Amill V, Appleton AA, Rosario-Villafañe V, Repollet-Carrer I, Borges-Rodríguez M, et al. Early childhood neurodevelopmental outcomes in children with prenatal Zika virus exposure: a cohort study in Puerto Rico. J Pediatr. 2022;247:38–e455.PubMedPubMedCentralCrossRef

Faiçal AV, de Oliveira JC, Oliveira JVV, de Almeida BL, Agra IA, Alcantara LCJ, et al. Neurodevelopmental delay in normocephalic children with in utero exposure to Zika virus. BMJ Paediatr Open. 2019;3(1):e000486.PubMedPubMedCentralCrossRef

Mulkey SB, Arroyave-Wessel M, Peyton C, Bulas DI, Fourzali Y, et al. Neurodevelopmental abnormalities in children with in utero Zika virus exposure without congenital Zika syndrome. JAMA Pediatr. 2020;174(3):269–76.PubMedPubMedCentralCrossRef

Nielsen-Saines K, Brasil P, Kerin T, Vasconcelos Z, Gabaglia CR, et al. Delayed childhood neurodevelopment and neurosensory alterations in the second year of life in a prospective cohort of ZIKV-exposed children. Nat Med. 2019;25(8):1213–7.PubMedPubMedCentralCrossRef

10.

2018–2019. National Survey of Children’s Health (NSCH) data query. https://www.childhealthdata.org/browse/survey/results?q=7965&r=1&g=812. Accessed 8 August 2023.

11.

Marbán-Castro E, Goncé A, Fumadó V, Romero-Acevedo L, Bardají A. Zika virus infection in pregnant women and their children: a review. Eur J Obstet Gynecol Reprod Biol. 2021;265:162–8.PubMedCrossRef

12.

Bayley N. Bayley Scales of Infant and Toddler Development: Administration Manual. 3rd ed. United States of America: The Psychological Corporation; 2006.

13.

Squires J, Twombley E, Bricker D, Potter L. Ages and stages questionnaires (ASQ): a parent-completed child monitoring system. 3rd ed. Baltimore, MD: Brookes; 2009.

14.

Squires J, Briker D, Twombly E. The ages and stages questionnaires: Social-Emotional (ASQ:SE) user’s guide. Baltimore: Paul H; 2002.

15.

Lopes Moreira ME, Nielsen-Saines K, Brasil P, Kerin T, Damasceno L, Pone M, et al. Neurodevelopment in infants exposed to Zika virus in utero. N Engl J Med. 2018;379(24):2377–9.PubMedPubMedCentralCrossRef

16.

Gerzson LR, de Almeida CS, Silva JHD, Feitosa MMA, de Oliveira LN, Schuler-Faccini L. Neurodevelopment of nonmicrocephalic children, after 18 months of life, exposed prenatally to Zika virus. J Child Neurol. 2020;35(4).

17.

Alger J, Cafferata ML, López R, Wiggins LD, Callejas A, Castillo M, et al. Neurodevelopmental assessment of normocephalic children born to Zika virus exposed and unexposed pregnant people. Pediatr Res. 2024;95(2):566–72.PubMedCrossRef

18.

Morawska A, Sanders M, Haslam D, Filus A, Fletcher R. Child Adjustment and parent efficacy scale (CAPES): development and initial validation of a parent report measure. Aust Psychol. 2014;44:241–52.CrossRef

19.

Seijo D, Tomé D, Sanmarco J, Morawska A, Fariña F. Spanish adaptation and validation of the Child Adjustment and parent efficacy scale. Sustainability. 2021;13(9):4647.CrossRef

20.

Kind AJH, Buckingham WR. Making Neighborhood-Disadvantage Metrics Accessible - The Neighborhood Atlas. N Engl J Med. 2018;378(26):2456–8.PubMedPubMedCentralCrossRef

21.

University of Wisconsin School of Medicine and Public Health. 2015 Area Deprivation Index v3.2. https://www.neighborhoodatlas.medicine.wisc.edu/. Accessed 8 August 2023.

22.

Martinez ML, Black M, Starr RH. Factorial structure of the Perceived Neighborhood Scale (PNS): a test of longitudinal invariance. J Commun Psychol. 2002;30(1):23–43.CrossRef

23.

Bradley RH, Caldwell BM. Home observation for measurement of the environment: a revision of the preschool scale. Am J Ment Defic. 1979;84(3):235–44.PubMed

24.

Epstein N, Bishop D, Levin S. The McMaster Model of Family Functioning. J Marital Fam Ther. 1978;4:19–31.CrossRef

25.

Barroilhet S, Cano-Prous A, Cervera-Enguix S, Forjaz MJ, Guillén-Grima F. A Spanish version of the Family Assessment device. Soc Psychiatry Psychiatr Epidemiol. 2009;44(12):1051–65.PubMedCrossRef

26.

Bickel G, Nord M, Price C, Hamilton W, Cook J. Guide to measuring household food security. Alexandria, VA, USA: US Department of Agriculture Food and Nutrition Service; 2000.

27.

Miller IW, Ryan CE, Keitner GI, Bishop DS, Epstein NB. The McMaster Approach to families: theory, assessment, treatment and research. J Family Ther. 2000;22(2):168–89.CrossRef

28.

Beck A, Steer R, Brown G. BDI-II Manual. San Antonio: The Psychological Corporation; 1996.

29.

Roque MP, Acle G, García M. Escala de resiliencia materna: Un estudio de validación en una muestra de madres con niños especiales. Rev Iberoam Diagn Ev. 2009;1(27):107–32.

30.

Cutrona C, Russel D. The provisions of social relationships and adaptation to stress. Adv Personal Relationships. 1987;1(1):37–67.

31.

Balistreri KS. Food insufficiency and children with special healthcare needs. Public Health. 2019;167:55–61.PubMedCrossRef

32.

Office of Disease Prevention and Health Promotion. Healthy People 2030. In: U.S. Department of Health and Human Services. https://health.gov/healthypeople. Accessed 8 August 2023.

33.

Poulain T, Vogel M, Kiess W. Review on the role of socioeconomic status in child health and development. Curr Opin Pediatr. 2020;32(2):308–14.PubMedCrossRef

34.

Schenck-Fontaine A, Ryan RM. Poverty, material hardship, and children’s outcomes: A nuanced understanding of material hardship in childhood. Child (Basel). 2022,9(7).

35.

Veldman SL, Jones RA, Chandler P, Robinson LE, Okely AD. Prevalence and risk factors of gross motor delay in pre-schoolers. J Paediatr Child Health. 2020;56(4):571–6.PubMedCrossRef

36.

Camden C, Héguy L, Casoli M, Roy M, Rivard L, Berbari J, Ppop Research Team CM. Preschoolers’ Developmental Profiles and School-Readiness in a Low-Income Canadian City: A Cross-Sectional Survey. Int J Environ Res Public Health. 2020;17(7).

37.

Hammer CS, Morgan P, Farkas G, Hillemeier M, Bitetti D, Maczuga S. Late talkers: a Population-based study of risk factors and School Readiness consequences. J Speech Lang Hear Res. 2017;60(3):607–26.PubMedPubMedCentralCrossRef

38.

Dea C, Gauvin L, Fournier M, Goldfeld S. Does Place Matter? An International comparison of early childhood development outcomes between the metropolitan areas of Melbourne, Australia and Montreal, Canada. Int J Environ Res Public Health. 2019;16(16):2915.PubMedPubMedCentralCrossRef

39.

González L, Cortés-Sancho R, Murcia M, Ballester F, Rebagliato M, Rodríguez-Bernal CL. The role of parental social class, education and unemployment on child cognitive development. Gac Sanit. 2020;34(1):51–60.PubMedCrossRef

40.

Schneider T, Linberg T. Development of socio-economic gaps in children’s language skills in Germany. Longit Life Course Stud. 2021;13(1):87–120.PubMedCrossRef

41.

Goldfeld S, O’Connor M, Chong S, Gray S, O’Connor E, Woolfenden S, et al. The impact of multidimensional disadvantage over childhood on developmental outcomes in Australia. Int J Epidemiol. 2018;47(5):1485–96.PubMedCrossRef

42.

Teymoori A, Côté SM, Jones BL, Nagin DS, Boivin M, Vitaro F, Orri M, Tremblay RE. Risk factors associated with boys’ and girls’ developmental trajectories of physical aggression from early childhood through early adolescence. JAMA Netw Open. 2018;1(8):e186364.PubMedPubMedCentralCrossRef

43.

Herrmann J, Vogel M, Pietzner D, Kroll E, Wagner O, Schwarz S, et al. Factors associated with the emotional health of children: high family income as a protective factor. Eur Child Adolesc Psychiatry. 2018;27(3):319–28.PubMedCrossRef

44.

Puerto Rico. Deficient on child and youth well-being by maintaining a 55% poverty level. https://www.juventudpr.org/blog/deficiente-puerto-rico-en-el-bienestar-de-la-ninez-y-la-juventud-al-mantener-un-nivel-de-pobreza-de-55. Accessed 10 August 2023.

45.

Food Stamps / Supplemental Nutrition Assistance Program (SNAP). https://data.census.gov/table?q=unemployment&t=Income+and+Poverty&tid=ACSST1Y2021.S1702. Accessed 10 August 2023.

46.

Black MM, Walker SP, Fernald LCH, Andersen CT, DiGirolamo AM, Lu C, et al. Early childhood development coming of age: science through the life course. Lancet. 2017;389(10064):77–90.PubMedCrossRef

47.

Gil JD, Ewerling F, Ferreira LZ, Barros AJ. Early childhood suspected developmental delay in 63 low- and middle-income countries: large within- and between-country inequalities documented using national health surveys. J Glob Health. 2020;10(1):010427.PubMedPubMedCentralCrossRef

48.

Cree RA, Bitsko RH, Robinson LR, Holbrook JR, Danielson ML, Smith C, et al. Health care, family, and community factors associated with mental, behavioral, and developmental disorders and poverty among children aged 2–8 years - United States, 2016. MMWR Morb Mortal Wkly Rep. 2018;67(50):1377–83.PubMedPubMedCentralCrossRef

49.

Food Security in the U.S. https://www.ers.usda.gov/topics/food-nutrition-assistance/food-security-in-the-u-s/. Accessed 10 August 2023.

50.

Jun S, Zeh MJ, Eicher-Miller HA, Bailey RL. Children’s dietary quality and micronutrient adequacy by food security in the household and among household children. Nutrients. 2019;11(5):965.PubMedPubMedCentralCrossRef

51.

Hobbs S, King C. The unequal impact of food insecurity on cognitive and behavioral outcomes among 5-year-old urban children. J Nutr Educ Behav. 2018;50(7):687–94.PubMedCrossRef

52.

Milner EM, Fiorella KJ, Mattah BJ, Bukusi E, Fernald LCH. Timing, intensity, and duration of household food insecurity are associated with early childhood development in Kenya. Matern Child Nutr. 2018;14(2):e12543.PubMedCrossRef

53.

Dean G, Vitolins MZ, Skelton JA, Ip EH, Lucas CB, Brown CL. The association of food insecurity with mental health in preschool-aged children and their parents. Pediatr Res. 2023;94(1):290–5.PubMedPubMedCentralCrossRef

54.

Thomas MMC, Miller DP, Morrissey TW. Food insecurity and child health. Pediatrics. 2019;144(4).

55.

Paquin V, Muckle G, Bolanis D, Courtemanche Y, Castellanos-Ryan N, Boivin M, et al. Longitudinal trajectories of food insecurity in childhood and their associations with mental health and functioning in adolescence. JAMA Netw Open. 2021;4(12):e2140085.PubMedPubMedCentralCrossRef

56.

Cook JT, Black M, Chilton M, Cutts D, Ettinger de Cuba S, Heeren TC, et al. Are food insecurity’s health impacts underestimated in the U.S. population? Marginal food security also predicts adverse health outcomes in young U.S. children and mothers. Adv Nutr. 2013;4(1):51–61.PubMedPubMedCentralCrossRef

57.

Barbeito-Andrés J, Schuler-Faccini L, Garcez PP. Why is congenital Zika syndrome asymmetrically distributed among human populations? PLoS Biol. 2018;16(8):e2006592.PubMedPubMedCentralCrossRef

58.

Entringer S, Buss C, Wadhwa PD. Prenatal stress, development, health and disease risk: a psychobiological perspective-2015 Curt Richter Award Paper. Psychoneuroendocrino. 2015;62:366–75.CrossRef

59.

Bruner CACE. Place, race, and poverty: building hope for children. Acad Pediatr. 2017;17(7S):S123–9.PubMedCrossRef

60.

Laplante DP, Brunet A, Schmitz N, Ciampi A, King S. Project Ice Storm: prenatal maternal stress affects cognitive and linguistic functioning in 5 1/2-year-old children. J Am Acad Child Adolesc Psychiatry. 2008;47(9):1063–72.PubMedCrossRef

61.

D’Souza S, Crawford CN, Buckley J, Underwood L, Peterson ER, Bird A, et al. Antenatal determinants of early childhood talking delay and behavioural difficulties. Infant Behav Dev. 2019;57:101388.PubMedCrossRef

62.

Haselbeck C, Niederberger U, Kulle A, Wache K, Brauner E, Gutermuth M, et al. Prenatal maternal distress seems to be associated with the infant’s temperament and motor development: an explorative study. J Neural Transm (Vienna). 2017;124(7):881–90.PubMedCrossRef

63.

Wei Q, Zou J, Ma X, Xiao X, Zhang Y, Shi H. Prospective associations between various prenatal exposures to maternal psychological stress and neurodevelopment in children within 24 months after birth. J Affect Disord. 2023;327:101–10.PubMedCrossRef

64.

Wu Y, Espinosa KM, Barnett SD, Kapse A, Quistorff JL, Lopez C, et al. Association of elevated maternal psychological distress, altered fetal brain, and offspring cognitive and social-emotional outcomes at 18 months. JAMA Netw Open. 2022;5(4):e229244.PubMedPubMedCentralCrossRef

65.

Duguay G, Garon-Bissonnette J, Lemieux R, Dubois-Comtois K, Mayrand K, Berthelot N. Socioemotional development in infants of pregnant women during the COVID-19 pandemic: the role of prenatal and postnatal maternal distress. Child Adolesc Psychiatry Ment Health. 2022;16(1):28.PubMedPubMedCentralCrossRef

66.

Tuovinen S, Lahti-Pulkkinen M, Girchenko P, Heinonen K, Lahti J, Reynolds RM, et al. Maternal antenatal stress and mental and behavioral disorders in their children. J Affect Disord. 2021;278:57–65.PubMedCrossRef

67.

Ahmad SI, Shih EW, LeWinn KZ, Rivera L, Graff JC, Mason WA, et al. Intergenerational transmission of effects of women’s stressors during pregnancy: child psychopathology and the protective role of parenting. Front Psychiatry. 2022;13:838535.PubMedPubMedCentralCrossRef

68.

Foss S, Petty CR, Howell C, Mendonca J, Bosse A, Waber DP, et al. Associations among maternal lifetime trauma, psychological symptoms in pregnancy, and infant stress reactivity and regulation. Dev Psychopathol. 2023;35(4):1714–31.PubMedCrossRef

69.

Masten AS. Resilience in developing systems: progress and promise as the fourth wave rises. Dev Psychopathol. 2007;19(3):921–30.PubMedCrossRef

70.

Southwick SM, Bonanno GA, Masten AS, Panter-Brick C, Yehuda R. Resilience definitions, theory, and challenges: interdisciplinary perspectives. Eur J Psychotraumatol. 2014;1;5.

71.

Kapogiannis BG, Chakhtoura N, Hazra R, Spong CY. Bridging knowledge gaps to Understand how Zika Virus exposure and infection affect Child Development. JAMA Pediatr. 2017;171(5):478–85.PubMedCrossRef

72.

Bethell CD, Gombojav N, Whitaker RC. Family resilience and connection promote flourishing among US children, even amid adversity. Health Aff (Millwood). 2019;38(5):729–37.PubMedCrossRef

73.

Salinas J, O’Donnell A, Kojis DJ, Pase MP, DeCarli C, Rentz DM, et al. Association of social support with brain volume and cognition. JAMA Netw Open. 2021;4(8):e2121122.PubMedPubMedCentralCrossRef

74.

Blackmon K, Evans R, Fernandes M, Landon B, Noel T, Macpherson C, et al. Neurodevelopment in normocephalic children with and without prenatal Zika virus exposure. Arch Dis Child. 2022;107(3):244–50.PubMedCrossRef

Title: Associations between the social environment and early childhood developmental outcomes of Puerto Rican children with prenatal Zika virus exposure: a cross-sectional study
Authors: Mary Rodríguez-Rabassa
Allison A. Appleton
Viviana Rosario-Villafañe
Irelis Repollet-Carrer
Marilyn Borges-Rodríguez
Lydiet Dedós-Peña
Marielly González
Paola Velázquez-González
Kamalich Muniz-Rodriguez
Claudia Mántaras-Ortiz
Vanessa Rivera-Amill
Odette Olivieri-Ramos
Luisa I. Alvarado-Domenech
Publication date: 01-12-2024
Publisher: BioMed Central
Keyword: Zika Virus
Published in: BMC Pediatrics / Issue 1/2024
Electronic ISSN: 1471-2431
DOI: https://doi.org/10.1186/s12887-024-04806-y

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Associations between the social environment and early childhood developmental outcomes of Puerto Rican children with prenatal Zika virus exposure: a cross-sectional study

Abstract

Background

Study design

Results

Conclusions

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Background

Study design

Results

Conclusions

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